Interactions between nitrous oxide and tissue plasminogen activator in a rat model of thromboembolic stroke

Anesthesiology

Volumn 115, Issue 5, 2011, Pages 1044-1053

  Haelewyn, Benoît ^a   David, Hélène N ^b,c   Colloc'H, Nathalie ^a   Colomb Jr , Denis G ^d,e   Risso, Jean Jacques ^f   Abraini, Jacques H ^a,b  

^a UNIVERSITÉ DE CAEN   (France)

^b UNIVERSITÉ LAVAL   (Canada)

^c CENTRE DE RECHERCHE DE L INSTITUT UNIVERSITAIRE EN SANTÉ MENTALE DE QUÉBEC   (Canada)

^d CNRS   (France)

^e Navy Experimental Diving Unit   (United States)

^f INSTITUT DE RECHERCHE BIOMÉDICALE DES ARMÉES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALTEPLASE; NITROUS OXIDE; XENON;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN HEMORRHAGE; BRAIN ISCHEMIA; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG BINDING; DRUG EFFECT; DRUG INHIBITION; ENZYME ACTIVITY; FIBRINOLYSIS; FIBRINOLYTIC THERAPY; IN VITRO STUDY; MALE; MOLECULAR MODEL; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; THROMBOEMBOLIC ACUTE ISCHEMIC STROKE; THROMBOEMBOLISM;

EID: 80054975030     PISSN: 00033022     EISSN: 15281175     Source Type: Journal    
DOI: 10.1097/ALN.0b013e3182342860     Document Type: Article

References (58)

1. Lijnen HR, Hoylaerts M, Collen D: Isolation and characterization of a human plasma protein with affinity for the lysine binding sites in plasminogen. Role in the regulation of fibrinolysis and identification as histidine-rich glycoprotein. J Biol Chem 1980; 255:10214-22 (Pubitemid 11214600)
2. Tissue plasminogen activator for acute ischemic stroke. The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. N Engl J Med 1995; 333:1581-7
3. Lees KR: ECASS-II: Intravenous alteplase in acute ischaemic stroke. European Co-operative Acute Stroke Study-II. Lancet 1999; 353:65-6
4. Hacke W, Kaste M, Bluhmki E, Brozman M, Dávalos A, Guidetti D, Larrue V, Lees KR, Medeghri Z, Machnig T, Schneider D, von Kummer R, Wahlgren N, Toni D, ECASS Investigators: Thrombolysis with alteplase 3 to 4.5 hours after acute ischemic stroke. N Engl J Med 2008; 359:1317-29
5. The NINDS t-PA Stroke Study Group: Intracerebral hemorrhage after intravenous t-PA therapy for ischemic stroke. Stroke 1997; 28:2109-18
6. Kidwell CS, Latour L, Saver JL, Alger JR, Starkman S, Duckwiler G, Jahan R, Vinuela F, UCLA Thrombolysis Investigators, Kang DW, Warach S: Thrombolytic toxicity: Blood brain barrier disruption in human ischemic stroke. Cerebrovasc Dis 2008; 25:338-43 (Pubitemid 351555857)
7. Yepes M, Roussel BD, Ali C, Vivien D: Tissue-type plasminogen activator in the ischemic brain: More than a thrombolytic. Trends Neurosci 2009; 32:48-55
8. Dirnagl U, Iadecola C, Moskowitz MA: Pathobiology of ischaemic stroke: An integrated view. Trends Neurosci 1999; 22:391-7 (Pubitemid 29453643)
9. Lo EH, Moskowitz MA, Jacobs TP: Exciting, radical, suicidal: How brain cells die after stroke. Stroke 2005; 36:189-92 (Pubitemid 40170779)
10. Lee JM, Zipfel GJ, Choi DW: The changing landscape of ischaemic brain injury mechanisms. Nature 1999; 399:A7-14 (Pubitemid 29295654)
11. Olney JW, Labruyere J, Wang G, Wozniak DF, Price MT, Sesma MA: NMDA antagonist neurotoxicity: Mechanism and prevention. Science 1991; 254:1515-8 (Pubitemid 21917493)
12. Davis SM, Lees KR, Albers GW, Diener HC, Markabi S, Karlsson G, Norris J: Selfotel in acute ischemic stroke: Possible neurotoxic effects of an NMDA antagonist. Stroke 2000; 31:347-54 (Pubitemid 30078164)
13. Kaur J, Zhao Z, Klein GM, Lo EH, Buchan AM: The neurotoxicity of tissue plasminogen activator? J Cereb Blood Flow Metab 2004; 24:945-63 (Pubitemid 39223619)
14. Jevtović-Todorović V, Todorović SM, Mennerick S, Powell S, Dikranian K, Benshoff N, Zorumski CF, Olney JW: Nitrous oxide (laughing gas) is an NMDA antagonist, neuroprotectant and neurotoxin. Nat Med 1998; 4:460-3 (Pubitemid 28212764)
15. Franks NP, Dickinson R, de Sousa SL, Hall AC, Lieb WR: How does xenon produce anaesthesia? Nature 1998; 396:324 (Pubitemid 28557385)
16. Yamakura T, Harris RA: Effects of gaseous anesthetics nitrous oxide and xenon on ligand-gated ion channels. Comparison with isoflurane and ethanol. Anesthesiology 2000; 93:1095-101
17. David HN, Ansseau M, Lemaire M, Abraini JH: Nitrous oxide and xenon prevent amphetamine-induced carrier-mediated dopamine release in a memantine-like fashion and protect against behavioral sensitization. Biol Psychiatry 2006; 60:49-57
18. +channels are a novel target for the anesthetic gases xenon, nitrous oxide, and cyclopropane. Mol Pharmacol 2004; 65:443-52 (Pubitemid 38134273)
19. Colloc'h N, Sopkova-de Oliveira Santos J, Retailleau P, Vivarès D, Bonneté F, Langlois d'Estainto B, Gallois B, Brisson A, Risso JJ, Lemaire M, Prangé T, Abraini JH: Protein crystallography under xenon and nitrous oxide pressure: Comparison with in vivo pharmacology studies and implications for the mechanism of inhaled anesthetic action. Biophys J 2007; 92:217-24 (Pubitemid 46055205)
20. Marassio G, Prangé T, David HN, Santos JS, Gabison L, Delcroix N, Abraini JH, Colloc'h N: Pressure-response analysis of anesthetic gases xenon and nitrous oxide on urate oxidase: A crystallographic study. FASEB J 2011; 25:2266-75
21. David HN, Leveille F, Chazalviel L, MacKenzie ET, Buisson A, Lemaire M, Abraini JH: Reduction of ischemic brain damage by nitrous oxide and xenon. J Cereb Blood Flow Metab 2003; 23:1168-73 (Pubitemid 37229520)
22. Abraini JH, David HN, Lemaire M: Potentially neuroprotective and therapeutic properties of nitrous oxide and xenon. Ann N Y Acad Sci 2005; 1053:289-300 (Pubitemid 43031108)
23. Haelewyn B, David HN, Rouillon C, Chazalviel L, Lecocq M, Risso JJ, Lemaire M, Abraini JH: Neuroprotection by nitrous oxide: Facts and evidence. Crit Care Med 2008; 36:2651-9
24. David HN, Haelewyn B, Rouillon C, Lecoq M, Chazalviel L, Apiou G, Risso JJ, Lemaire M, Abraini JH: Neuroprotective effects of xenon: A therapeutic window of opportunity in rats subjected to transient cerebral ischemia. FASEB J 2008; 22:1275-86 (Pubitemid 351519980)
25. Homi HM, Yokoo N, Ma D, Warner DS, Franks NP, Maze M, Grocott HP: The neuroprotective effect of xenon administration during transient middle cerebral artery occlusion in mice. Anesthesiology 2003; 99:876-81 (Pubitemid 37186078)
26. Dingley J, Tooley J, Porter H, Thoresen M: Xenon provides short-term neuroprotection in neonatal rats when administered after hypoxia-ischemia. Stroke 2006; 37:501-6 (Pubitemid 43732014)
27. Ma D, Hossain M, Chow A, Arshad M, Battson RM, Sanders RD, Mehmet H, Edwards AD, Franks NP, Maze M: Xenon and hypothermia combine to provide neuroprotection from neonatal asphyxia. Ann Neurol 2005; 58:182-93 (Pubitemid 41098876)
28. Ma D, Yang H, Lynch J, Franks NP, Maze M, Grocott HP: Xenon attenuates cardiopulmonary bypass-induced neurologic and neurocognitive dysfunction in the rat. Anesthesiology 2003; 98:690-8 (Pubitemid 36262596)
29. David HN, Haelewyn B, Risso JJ, Colloc'h N, Abraini JH: Xenon is an inhibitor of tissue-plasminogen activator: Adverse and beneficial effects in a rat model of thromboembolic stroke. J Cereb Blood Flow Metab 2010; 30:718-28
30. Renatus M, Bode W, Huber R, Stürzebecher J, Prasa D, Fischer S, Kohnert U, Stubbs MT: Structural mapping of the active site specificity determinants of human tissue-type plasminogen activator. Implications for the design of low molecular weight substrates and inhibitors. J Biol Chem 1997; 272:21713-9 (Pubitemid 27382784)
31. Haelewyn B, Risso JJ, Abraini JH: Human recombinant tissueplasminogen activator (alteplase): Why not use the 'human' dose for stroke studies in rats? J Cereb Blood Flow Metab 2010; 30:900-3
32. Henninger N, Küppers-Tiedt L, Sicard KM, Günther A, Schneider D, Schwab S: Neuroprotective effect of hyperbaric oxygen therapy monitored by MR-imaging after embolic stroke in rats. Exp Neurol 2006; 201:316-23 (Pubitemid 44344224)
33. Haelewyn B, Alix P, Maubert E, Abraini JH: NMDA-induced striatal brain damage and time-dependence reliability of thionin staining in rats. J Neurosci Methods 2008; 168:479-82
34. Henninger N, Bratane BT, Bastan B, Bouley J, Fisher M: Normobaric hyperoxia and delayed tPA treatment in a rat embolic stroke model. J Cereb Blood Flow Metab 2009; 29:119-29
35. Schiltz M, Fourme R, Broutin I, Prangé T: The catalytic site of serine proteinases as a specific binding cavity for xenon. Structure 1995; 3:309-16
36. Marassio G, Prangé T, Vallone B, Abraini JH, Colloc'h N: Anesthetic gas xenon and nitrous oxide: Same physiological target and same binding site in proteins. 3rd International Symposium on Diffraction Structural Biology, Orsay, France, May 25-28, 2010
37. Christou I, Alexandrov AV, Burgin WS, Wojner AW, Felberg RA, Malkoff M, Grotta JC: Timing of recanalization after tissue plasminogen activator therapy determined by transcranial doppler correlates with clinical recovery from ischemic stroke. Stroke 2000; 31:1812-6 (Pubitemid 30620455)
38. Delgado-Mederos R, Rovira A, Alvarez-Sabín J, Ribó M, Munuera J, Rubiera M, Santamarina E, Maisterra O, Delgado P, Montaner J, Molina CA: Speed of tPA-induced clot lysis predicts DWI lesion evolution in acute stroke. Stroke 2007; 38:955-60 (Pubitemid 46568458)
39. Tsirka SE, Gualandris A, Amaral DG, Strickland S: Excitotoxininduced neuronal degeneration and seizure are mediated by tissue plasminogen activator. Nature 1995; 377:340-4
40. Wang YF, Tsirka SE, Strickland S, Stieg PE, Soriano SG, Lipton SA: Tissue plasminogen activator (tPA) increases neuronal damage after focal cerebral ischemia in wild-type and tPAdeficient mice. Nat Med 1998; 4:228-31 (Pubitemid 28138083)
41. Tyson GW, Teasdale GM, Graham DI, McCulloch J: Focal cerebral ischemia in the rat: Topography of hemodynamic and histopathological changes. Ann Neurol 1984; 15:559-67 (Pubitemid 14124609)
42. Reinstrup P, Ryding E, Ohlsson T, Sandell A, Erlandsson K, Ljunggren K, Salford LG, Strand S, Uski T: Regional cerebral metabolic rate (positron emission tomography) during inhalation of nitrous oxide 50% in humans. Br J Anaesth 2008; 100:66-71 (Pubitemid 351773422)
43. Johansson BB, Linder LE: Cerebrovascular permeability to protein in the rat during nitrous oxide anaesthesia at various blood pressure levels. Acta Anaesthesiol Scand 1978; 22: 463-6 (Pubitemid 8390097)
44. Remsen LG, Pagel MA, McCormick CI, Fiamengo SA, Sexton G, Neuwelt EA: The influence of anesthetic choice, PaCO2, and other factors on osmotic blood-brain barrier disruption in rats with brain tumor xenografts. Anesth Analg 1999; 88:559-67 (Pubitemid 29109022)
45. Frietsch T, Bogdanski R, Blobner M, Werner C, Kuschinsky W, Waschke KF: Effects of xenon on cerebral blood flow and cerebral glucose utilization in rats. Anesthesiology 2001; 94:290-7 (Pubitemid 32125919)
46. Schmidt M, Marx T, Papp-Jambor C, Schirmer U, Reinelt H: Effect of xenon on cerebral autoregulation in pigs. Anaesthesia 2002; 57:960-6 (Pubitemid 35203326)
47. Laitio RM, Kaisti KK, Låangsjö JW, Aalto S, Salmi E, Maksimow A, Aantaa R, Oikonen V, Sipilä H, Parkkola R, Scheinin H: Effects of xenon anesthesia on cerebral blood flow in humans: A positron emission tomography study. Anesthesiology 2007; 106:1128-33 (Pubitemid 46828165)
48. Field LM, Dorrance DE, Krzeminska EK, Barsoum LZ: Effect of nitrous oxide on cerebral blood flow in normal humans. Br J Anaesth 1993; 70:154-9 (Pubitemid 23042087)
49. Nakanishi O, Ishikawa T, Imamura Y, Hirakawa T: Inhibition of cerebral metabolic and circulatory responses to nitrous oxide by 6-hydroxydopamine in dogs. Can J Anaesth 1997; 44:1008-13 (Pubitemid 28022624)
50. Yokoo N, Sheng H, Mixco J, Homi HM, Pearlstein RD, Warner DS: Intraischemic nitrous oxide alters neither neurologic nor histologic outcome: A comparison with dizocilpine. Anesth Analg 2004; 99:896-903 (Pubitemid 39100386)
51. Abraini JH, David HN, MacKenzie ET, Lemaire M: Postischemic nitrous oxide alone versus intraischemic nitrous oxide in the presence of isoflurane: What it may change for neuroprotection against cerebral stroke in the rat. Anesth Analg 2005; 101:614 (Pubitemid 41045266)
52. Sugaya T, Kitani Y: Nitrous oxide attenuates the protective effect of isoflurane on microtubule-associated protein2 degradation during forebrain ischemia in the rat. Brain Res Bull 1997; 44:307-9 (Pubitemid 27413735)
53. Nasu I, Yokoo N, Takaoka S, Takata K, Hoshikawa T, Okada M, Miura Y: The dose-dependent effects of isoflurane on outcome from severe forebrain ischemia in the rat. Anesth Analg 2006; 103:413-8 (Pubitemid 44140644)
54. Sanders RD, Ma D, Maze M: Anaesthesia induced neuroprotection. Best Pract Res Clin Anaesthesiol 2005; 19:461-74 (Pubitemid 40753812)
55. Olney JW, Farber NB, Wozniak DF, Jevtovic-Todorovic V, Ikonomidou C: Environmental agents that have the potential to trigger massive apoptotic neurodegeneration in the developing brain. Environ Health Perspect 2000; 108(suppl 3): 383-8 (Pubitemid 30466160)
56. Istaphanous GK, Howard J, Nan X, Hughes EA, McCann JC, McAuliffe JJ, Danzer SC, Loepke AW: Comparison of the neuroapoptotic properties of equipotent anesthetic concentrations of desflurane, isoflurane, or sevoflurane in neonatal mice. Anesthesiology 2011; 114:578-87
57. Kollmar R, Blank T, Han JL, Georgiadis D, Schwab S: Different degrees of hypothermia after experimental stroke: Shortand long-term outcome. Stroke 2007; 38:1585-9 (Pubitemid 46684178)
58. Fisher CM: Lacunes: Small, deep cerebral infarcts. 1965. Neurology 1998; 50:841-52